Proteomic analysis of protein tyrosine nitration after ischemia reperfusion injury: Mitochondria as the major target

Biochimica et Biophysica Acta - Proteins and Proteomics

Volumn 1794, Issue 3, 2009, Pages 476-485

  Liu, Bin ^a   Tewari, Arun K ^a   Zhang, Liwen ^b   Green Church, Kari B ^b   Zweier, Jay L ^a   Chen, Yeong Renn ^a   He, Guanglong ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b OHIO STATE UNIVERSITY   (United States)

Author keywords

Energy metabolism; Nitric oxide; Oxidative phosphorylation; Oxygen consumption; Peroxynitrite

Indexed keywords

MITOCHONDRIAL PROTEIN; PROTON TRANSPORTING ADENOSINE TRIPHOSPHATE SYNTHASE; TYROSINE; VOLTAGE DEPENDENT ANION CHANNEL;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTERY LIGATION; ARTICLE; CONTROLLED STUDY; ISCHEMIA; LEFT ANTERIOR DESCENDING CORONARY ARTERY; LIQUID CHROMATOGRAPHY; MALE; MITOCHONDRION; MOUSE; NITRATION; NONHUMAN; OXIDATIVE PHOSPHORYLATION; PRIORITY JOURNAL; PROTEOMICS; REPERFUSION INJURY; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

ANIMALS; BLOTTING, WESTERN; ELECTRON TRANSPORT COMPLEX I; ELECTROPHORESIS, GEL, TWO-DIMENSIONAL; MICE; MITOCHONDRIA, HEART; MITOCHONDRIAL PROTEINS; MYOCARDIAL REPERFUSION INJURY; NITRATES; PROTEOMICS; TANDEM MASS SPECTROMETRY; TYROSINE;

EID: 59549106445     PISSN: 15709639     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bbapap.2008.12.008     Document Type: Article

References (52)

1. Ferdinandy P., and Schulz R. Nitric oxide, superoxide, and peroxynitrite in myocardial ischaemia-reperfusion injury and preconditioning. Br. J. Pharmacol. 138 (2003) 532-543
2. Hare J.M., and Colucci W.S. Role of nitric oxide in the regulation of myocardial function. Prog. Cardiovasc. Dis. 38 (1995) 155-166
3. Valdez L.B., Alvarez S., Arnaiz S.L., Schopfer F., Carreras M.C., Poderoso J.J., and Boveris A. Reactions of peroxynitrite in the mitochondrial matrix. Free Radic. Biol. Med. 29 (2000) 349-356
4. Peluffo G., and Radi R. Biochemistry of protein tyrosine nitration in cardiovascular pathology. Cardiovasc. Res. 75 (2007) 291-302
5. Wang P., and Zweier J.L. Measurement of nitric oxide and peroxynitrite generation in the postischemic heart. Evidence for peroxynitrite-mediated reperfusion injury. J. Biol. Chem. 271 (1996) 29223-29230
6. Zweier J.L., Kuppusamy P., Williams R., Rayburn B.K., Smith D., Weisfeldt M.L., and Flaherty J.T. Measurement and characterization of postischemic free radical generation in the isolated perfused heart. J. Biol. Chem. 264 (1989) 18890-18895
7. Xie Y.W., Kaminski P.M., and Wolin M.S. Inhibition of rat cardiac muscle contraction and mitochondrial respiration by endogenous peroxynitrite formation during posthypoxic reoxygenation. Circ. Res. 82 (1998) 891-897
8. Xie Y.W., and Wolin M.S. Role of nitric oxide and its interaction with superoxide in the suppression of cardiac muscle mitochondrial respiration. Involvement in response to hypoxia/reoxygenation. Circulation 94 (1996) 2580-2586
9. Zhao X., He G., Chen Y.R., Pandian R.P., Kuppusamy P., and Zweier J.L. Endothelium-derived nitric oxide regulates postischemic myocardial oxygenation and oxygen consumption by modulation of mitochondrial electron transport. Circulation 111 (2005) 2966-2972
10. Xu Y., Liu B., Zweier J.L., and He G. Formation of hydrogen peroxide and reduction of peroxynitrite via dismutation of superoxide at reperfusion enhances myocardial blood flow and oxygen consumption in postischemic mouse heart. J. Pharmacol. Exp. Ther. 327 (2008) 402-410
11. Levrand S., Vannay-Bouchiche C., Pesse B., Pacher P., Feihl F., Waeber B., and Liaudet L. Peroxynitrite is a major trigger of cardiomyocyte apoptosis in vitro and in vivo. Free Radic. Biol. Med. 41 (2006) 886-895
12. Pacher P., Beckman J.S., and Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol. Rev. 87 (2007) 315-424
13. Murray J., Taylor S.W., Zhang B., Ghosh S.S., and Capaldi R.A. Oxidative damage to mitochondrial complex I due to peroxynitrite: identification of reactive tyrosines by mass spectrometry. J. Biol. Chem. 278 (2003) 37223-37230
14. MacMillan-Crow L.A., Crow J.P., and Thompson J.A. Peroxynitrite-mediated inactivation of manganese superoxide dismutase involves nitration and oxidation of critical tyrosine residues. Biochemistry 37 (1998) 1613-1622
15. Aslan M., Ryan T.M., Townes T.M., Coward L., Kirk M.C., Barnes S., Alexander C.B., Rosenfeld S.S., and Freeman B.A. Nitric oxide-dependent generation of reactive species in sickle cell disease. Actin tyrosine induces defective cytoskeletal polymerization. J. Biol. Chem. 278 (2003) 4194-4204
16. Eiserich J.P., Estevez A.G., Bamberg T.V., Ye Y.Z., Chumley P.H., Beckman J.S., and Freeman B.A. Microtubule dysfunction by posttranslational nitrotyrosination of alpha-tubulin: a nitric oxide-dependent mechanism of cellular injury. Proc. Natl. Acad. Sci. USA 96 (1999) 6365-6370
17. Takakura K., Beckman J.S., MacMillan-Crow L.A., and Crow J.P. Rapid and irreversible inactivation of protein tyrosine phosphatases PTP1B, CD45, and LAR by peroxynitrite. Arch. Biochem. Biophys. 369 (1999) 197-207
18. Yakovlev V.A., Barani I.J., Rabender C.S., Black S.M., Leach J.K., Graves P.R., Kellogg G.E., and Mikkelsen R.B. Tyrosine nitration of IkappaBalpha: a novel mechanism for NF-kappaB activation. Biochemistry 46 (2007) 11671-11683
19. Oury T.D., Tatro L., Ghio A.J., and Piantadosi C.A. Nitration of tyrosine by hydrogen peroxide and nitrite. Free Radic. Res. 23 (1995) 537-547
20. Ko J., Yan J., Zhu L., Qi Y., and Subtilisin Q.K. A fibrinolytic enzyme, inhibits the exogenous nitrite and hydrogen peroxide induced protein nitration, in vitro and in vivo. J. Biochem. Mol. Biol. 38 (2005) 577-583
21. Crow J.P., and Ischiropoulos H. Detection and quantitation of nitrotyrosine residues in proteins: in vivo marker of peroxynitrite. Methods Enzymol. 269 (1996) 185-194
22. Kuhn D.M., Sakowski S.A., Sadidi M., and Geddes T.J. Nitrotyrosine as a marker for peroxynitrite-induced neurotoxicity: the beginning or the end of the end of dopamine neurons?. J. Neurochem. 89 (2004) 529-536
23. MacMillan-Crow L.A., Crow J.P., Kerby J.D., Beckman J.S., and Thompson J.A. Nitration and inactivation of manganese superoxide dismutase in chronic rejection of human renal allografts. Proc. Natl. Acad. Sci. USA 93 (1996) 11853-11858
24. Turko I.V., Li L., Aulak K.S., Stuehr D.J., Chang J.Y., and Murad F. Protein tyrosine nitration in the mitochondria from diabetic mouse heart. Implications to dysfunctional mitochondria in diabetes. J. Biol. Chem. 278 (2003) 33972-33977
25. Hong S.J., Gokulrangan G., and Schoneich C. Proteomic analysis of age dependent nitration of rat cardiac proteins by solution isoelectric focusing coupled to nanoHPLC tandem mass spectrometry. Exp. Gerontol. 42 (2007) 639-651
26. Kanski J., Behring A., Pelling J., and Schoneich C. Proteomic identification of 3-nitrotyrosine-containing rat cardiac proteins: effects of biological aging. Am. J. Physiol. Heart Circ. Physiol. 288 (2005) H371-381
27. Zhu X., Liu B., Zhou S., Chen Y.R., Deng Y., Zweier J.L., and He G. Ischemic preconditioning prevents in vivo hyperoxygenation in postischemic myocardium with preservation of mitochondrial oxygen consumption. Am. J. Physiol. Heart Circ. Physiol. 293 (2007) H1442-H1450
28. Lowry O.H., Rosebrough N.J., Farr A.L., and Randall R.J. Protein measurement with the folin phenol reagent. J. Biol. Chem. 193 (1951) 265-275
29. Salinovich O., and Montelaro R.C. Reversible staining and peptide mapping of proteins transferred to nitrocellulose after separation by sodium dodecylsulfate-polyacrylamide gel electrophoresis. Anal. Biochem. 156 (1986) 341-347
30. Chen C.L., Zhang L., Yeh A., Chen C.A., Green-Church K.B., Zweier J.L., and Chen Y.R. Site-specific S-glutathiolation of mitochondrial NADH ubiquinone reductase. Biochemistry 46 (2007) 5754-5765
31. Vinogradov A.D., and King T.E. The Keilin-Hartree heart muscle preparation. Methods Enzymol. 55 (1979) 118-127
32. Radi R., Rodriguez M., Castro L., and Telleri R. Inhibition of mitochondrial electron transport by peroxynitrite. Arch. Biochem. Biophys. 308 (1994) 89-95
33. Radi R., Cassina A., Hodara R., Quijano C., and Castro L. Peroxynitrite reactions and formation in mitochondria. Free Radic. Biol. Med. 33 (2002) 1451-1464
34. Gustafsson A.B., and Gottlieb R.A. Heart mitochondria: gates of life and death. Cardiovasc. Res. 77 (2008) 334-343
35. Ischiropoulos H. Biological selectivity and functional aspects of protein tyrosine nitration. Biochem. Biophys. Res. Commun. 305 (2003) 776-783
36. Schoneich C., and Sharov V.S. Mass spectrometry of protein modifications by reactive oxygen and nitrogen species. Free Radic. Biol. Med. 41 (2006) 1507-1520
37. Aulak K.S., Koeck T., Crabb J.W., and Stuehr D.J. Dynamics of protein nitration in cells and mitochondria. Am. J. Physiol. Heart Circ. Physiol. 286 (2004) H30-H38
38. Koeck T., Fu X., Hazen S.L., Crabb J.W., Stuehr D.J., and Aulak K.S. Rapid and selective oxygen-regulated protein tyrosine denitration and nitration in mitochondria. J. Biol. Chem. 279 (2004) 27257-27262
39. Koeck T., Stuehr D.J., and Aulak K.S. Mitochondria and regulated tyrosine nitration. Biochem. Soc. Trans. 33 (2005) 1399-1403
40. Grune T., Reinheckel T., and Davies K.J. Degradation of oxidized proteins in mammalian cells. Faseb J. 11 (1997) 526-534
41. Sazanov L.A., and Hinchliffe P. Structure of the hydrophilic domain of respiratory complex I from Thermus thermophilus. Science 311 (2006) 1430-1436
42. Crofts A.R. Proton-coupled electron transfer at the Qo-site of the bc1 complex controls the rate of ubihydroquinone oxidation. Biochim. Biophys. Acta 1655 (2004) 77-92
43. Leyva J.A., Bianchet M.A., and Amzel L.M. Understanding ATP synthesis: structure and mechanism of the F1-ATPase (review). Mol. Membr. Biol. 20 (2003) 27-33
44. Chen C.L., Chen J., Rawale S., Varadharaj S., Kaumaya P.P., Zweier J.L., and Chen Y.R. Protein tyrosine nitration of the flavin subunit is associated with oxidative modification of mitochondrial complex II in the post-ischemic myocardium. J. Biol. Chem. 283 (2008) 27991-28003
45. Ghafourifar P., and Colton C.A. Compartmentalized nitrosation and nitration in mitochondria. Antioxid. Redox Signal. 5 (2003) 349-354
46. Iwata S., Lee J.W., Okada K., Lee J.K., Iwata M., Rasmussen B., Link T.A., Ramaswamy S., and Jap B.K. Complete structure of the 11-subunit bovine mitochondrial cytochrome bc1 complex. Science 281 (1998) 64-71
47. Han D., Antunes F., Canali R., Rettori D., and Cadenas E. Voltage-dependent anion channels control the release of the superoxide anion from mitochondria to cytosol. J. Biol. Chem. 278 (2003) 5557-5563
48. Witze E.S., Old W.M., Resing K.A., and Ahn N.G. Mapping protein post-translational modifications with mass spectrometry. Nat. Methods 4 (2007) 798-806
49. Zhan X., and Desiderio D.M. The human pituitary nitroproteome: detection of nitrotyrosyl-proteins with two-dimensional Western blotting, and amino acid sequence determination with mass spectrometry. Biochem. Biophys. Res. Commun. 325 (2004) 1180-1186
50. Irie Y., Saeki M., Kamisaki Y., Martin E., and Murad F. Histone H1.2 is a substrate for denitrase, an activity that reduces nitrotyrosine immunoreactivity in proteins. Proc. Natl. Acad. Sci. USA 100 (2003) 5634-5639
51. Paradies G., Petrosillo G., Pistolese M., Di Venosa N., Federici A., and Ruggiero F.M. Decrease in mitochondrial complex I activity in ischemic/reperfused rat heart: involvement of reactive oxygen species and cardiolipin. Circ. Res. 94 (2004) 53-59
52. Hardy L., Clark J.B., Darley-Usmar V.M., Smith D.R., and Stone D. Reoxygenation-dependent decrease in mitochondrial NADH:CoQ reductase (Complex I) activity in the hypoxic/reoxygenated rat heart. Biochem. J. 274 Pt. 1 (1991) 133-137